bioRxiv Science⌕ Search

Biology subjects

Fitzpatrick, J. W.

Publications and source records attributed to Fitzpatrick, J. W..

13 recordsLinked to original sources

Indirect genetic effects across ontogeny in an avian cooperative breeder

Social interactions are ubiquitous in nature and have the potential to affect trait evolution, particularly in group-living animals such as cooperative breeders. Interactions among conspecific individuals can affect the amount of additive genetic variation for a trait when the phenotype of an individual is also affected by the genotype of its social partner(s) via indirect genetic effects. Thus, quantifying both direct and indirect genetic effects of social partners is critical for understanding and predicting evolutionary trajectories. While much is known about maternal indirect genetic effects, empirical estimates of indirect genetic effects from other social partners remain limited, particularly in wild populations. Here, we use animal models to assess the contribution of indirect genetic effects from all social partners in a family group (mothers, fathers, and helpers) on juvenile morphometric traits across ontogeny in the cooperatively-breeding Florida scrub-jay (Aphelocoma coerulescens). We found indirect genetic effects of helpers and fathers on nestling weight, but no indirect genetic effect of mothers. Across ontogeny, we found increasing additive genetic variation in both weight and tarsus length. Our study provides a comprehensive assessment of within-group indirect genetic effects in a cooperative breeder and highlights the importance of considering indirect genetic effects beyond maternal effects.

evolutionary biology↗

Sustained multigenerational fitness benefits of natural immigration

The fitness of immigrants and their descendants determines the effectiveness of gene flow. Genetic incompatibilities or outbreeding depression can limit the spread of novel alleles, while highly fit immigrant lineages can hasten introgression. These fitness effects of gene flow can also differ between generations as immigrant and resident haplotypes recombine. Understanding the genetic factors that shape immigrant fitness over multiple generations is increasingly important as habitat fragmentation threatens populations by reducing genetic variation and leading to increased levels of inbreeding. Few studies have measured the multigenerational fitness of immigrant lineages, especially within populations that had histories of high gene flow. We used 33 years of life history and pedigree data on a population of Florida scrub-jays (Aphelocoma coerulescens) with historically high immigration to quantify the fitness of immigrants and their descendants. We compared the fitness of immigrants and residents as well as their resulting descendants (F1, F2, etc.) to determine the composite genetic effects responsible for fitness differences. We found evidence of additive benefits of immigrant ancestry and heterosis driven by non-additive effects that persists for multiple generations. These results are promising for conservation efforts aiming to increase connectivity and illustrate the complex dynamics that determine the rates of introgression in natural populations.

evolutionary biology↗

Genome-wide associations of fitness components reveal antagonistic pleiotropy and sexual conflict in the Florida Scrub-Jay

Natural populations often exhibit substantial genetic variation in fitness-related traits, providing the raw material for adaptation. The persistence of high levels of genetic variation in the presence of genetic drift and directional selection has long puzzled evolutionary biologists1-3. Recent studies suggest that antagonistic pleiotropy may play a greater role than previously appreciated, highlighting the need for more empirical studies that consider both sexual antagonism and life-history trade-offs4. Here, we performed a comprehensive assessment of fitness trade-offs within and between sexes in an extensively monitored natural population of Florida Scrub-Jays (Aphelocoma coerulescens)5. We found significant additive genetic variance for female fitness and identified several loci associated with variation in survival, fecundity, and lifetime reproductive success. Many loci associated with multiple fitness components had antagonistic effects, particularly within males. Considering genome-wide polygenic effects, we found multiple genetic trade-offs both within and between sexes, especially when considering different fitness components between sexes. Comparing allele frequency trajectories for putatively pleiotropic loci demonstrated that antagonistic SNPs had smaller allele frequency changes than concordant SNPs. Our fine-scale dissection of fitness components reveals substantial antagonistic pleiotropy that affects short-term evolution, highlighting the importance of antagonistic selection in maintaining genetic variation over short time scales in nature.

evolutionary biology↗

Context-Dependent Fitness Outcomes of Helping in the Cooperatively-Breeding Florida Scrub-Jay (Aphelocoma coerulescens)

Cooperatively breeding species frequently live in family groups of related individuals, with helpers delaying their own reproduction and participating in alloparental care, predator vigilance, and territory defense. It remains challenging to disentangle the roles of the indirect fitness benefits of helping kin and the potential direct fitness benefits helpers receive in the evolution of cooperative breeding. While many studies test for associations between helper relatedness and helping effort, few estimate the realized fitness consequences of helping in relation to these factors. Understanding these fitness outcomes elucidates the selective forces that maintain helping behavior, whether through inclusive fitness gains by helping related individuals or as a means of gaining access to later direct fitness benefits. Using 29 years of extensive demographic data from a closely monitored population of Florida scrub-jays (Aphelocoma coerulescens), we quantified the effect of helpers on breeder survival, offspring survival, and nestling production and how these effects depend on relatedness and sex of helpers. We found that female breeder survival was significantly greater when more helpers were present and that offspring survival was greater when more male helpers were present on small territories. Neither effect of helpers depended on the relatedness between helpers and the individuals they helped. Our results suggest that helping behavior is highly context-dependent and varies based on the potential impact of helping and the direct fitness benefits helpers receive.

ecology↗

Comparative population pangenomes reveal unexpected complexity and fitness effects of structural variants

Structural variants (SVs) are widespread in vertebrate genomes, yet their evolutionary dynamics remain poorly understood. Using 45 long-read de novo genome assemblies and pangenome tools, we analyze SVs within three closely related species of North American jays (Aphelocoma, scrub-jays) displaying a 60-fold range in effective population size. We find rapid evolution of genome architecture, including [~]100 Mb variation in genome size driven by dynamic satellite landscapes with unexpectedly long (> 10 kb) repeat units and widespread variation in gene content, influencing gene expression. SVs exhibit slightly deleterious dynamics modulated by variant length and population size, with strong evidence of adaptive fixation only in large populations. Our results demonstrate how population size shapes the distribution of SVs and the importance of pangenomes to characterizing genomic diversity.

evolutionary biology↗

Whole-genome sequencing across space and time reveals impact of population decline and reduced gene flow in Florida Scrub-Jays

Whole-genome sequence data is proving to be highly informative about the past demography of free-living populations, and in the context of endangered species, it can provide a quantification of the genetic risk posed by reduced genetic diversity and inbreeding. Prior to 1920, the Florida scrub-jay (Aphelocoma coerulescens) had been widespread across Florida, but with the expansion of agriculture and human habitation, its population has declined by 95%, resulting in fragmentation into semi-isolated subpopulations. By sequencing 241 individuals sampled from five different regions and across two time points, this study quantifies a greater magnitude of loss of genetic diversity and greater levels of inbreeding in smaller and more isolated subpopulations. Consistent with population genetics theory, reduction in population size results in a dramatic loss of rare alleles, skewing the site frequency spectrum far from the expected equilibrium. Increased inbreeding in the smaller, more remote subpopulations is especially evident in the increased size and number of runs of homozygosity. The Florida scrub-jay displays limited dispersal, and habitat fragmentation has greatly reduced the magnitude of gene flow in the past 30 years, resulting in further decline of genetic diversity, especially in the peripheral populations. Analysis of these data is informative in guiding conservation efforts to retain genetic diversity and minimize the consequences of inbreeding in the Florida scrub-jay. HighlightsO_LIFive regional populations show distinct degrees of population isolation and decline. C_LIO_LIThere has been commensurate loss of genetic diversity, skewed site frequency spectra, reduced migration, and increased inbreeding (FROH). C_LIO_LIAs many state-wide populations decline, the smaller, more remote populations provide a glimpse into the future and a testbed for remediation approaches. C_LI

genomics↗

Lifetime fitness benefits of breeding site fidelity and low costs of inbreeding permit inbreeding tolerance in an avian cooperative breeder

Breeding with relatives often decreases individual fitness but can be mitigated via inbreeding avoidance mechanisms such as dispersal, mate-switching, and kin avoidance. Disentangling the effects of multiple mechanisms is challenging without detailed individual-level data and incomplete without considering all life stages. We leveraged 32 years of data from a population of Florida Scrub-Jays (Aphelocoma coerulescens) to investigate how dispersal and mate choice contribute to inbreeding risk across individuals lifetimes and quantify the associated fitness outcomes. We find that when mating is random, inbreeding is two-fold higher when dispersal is limited, but adding sex-biased dispersal significantly reduces inbreeding risk. Limited movement away from the breeding territory for later pairings (site fidelity) contributes more to higher-than-expected levels of inbreeding than limited natal dispersal. Within observed dispersal constraints, however, inbreeding is lower than expected under random mating, suggesting Florida Scrub-Jays actively avoid mating with relatives, especially first-order kin. Finally, males paired with close relatives and females who move farther for later pairings experience equivalently lower lifetime reproductive success. Breeders who move farther for first pairings have lower survival. Overall, our results show how variation in fitness tradeoffs and mate choice behavior across life stages affects inbreeding in a long-lived, social species.

animal behavior and cognition↗

A new high-quality genome assembly and annotation for the threatened Florida Scrub-Jay (Aphelocoma coerulescens)

The Florida Scrub-Jay (Aphelocoma coerulescens), a Federally Threatened, cooperatively-breeding bird, is an emerging model system in evolutionary biology and ecology. Extensive individual-based monitoring and genetic sampling for decades has yielded a wealth of data, allowing for the detailed study of social behavior, demography, and population genetics of this natural population. Here, we report a linkage map and a chromosome-level genome assembly and annotation for a female Florida Scrub-Jay made with long-read sequencing technology, chromatin conformation data, and the linkage map. We constructed a linkage map comprising 4,468 SNPs that had 34 linkage groups and a total sex-averaged autosomal genetic map length of 2446.78 cM. The new genome assembly is 1.32 Gb in length, consisting of 33 complete or near-complete autosomes and the sex chromosomes (ZW). This highly contiguous assembly has an N50 of 68 Mb and a Benchmarking Universal Single-Copy Orthologs (BUSCO) completeness score of 97.1% with respect to the Aves database. The annotated gene set has a BUSCO transcriptome completeness score of 95.5% and 18,051 identified protein-coding genes, 92.2% of which have associated functional annotations. This new, high-quality genome assembly and linkage map of the Florida Scrub-Jay provides valuable tools for future research into the evolutionary dynamics of small, natural populations of conservation concern. ARTICLE SUMMARYWe present a new high-quality genome assembly and annotation for the Florida Scrub-Jay (Aphelocoma coerulescens), a Federally Threatened bird species. In comparison to other genome assemblies of this species, our assembly is the first to be made using long-read sequencing technology and is the first generated from a female individual. We also constructed the first linkage map for this species using a population pedigree. Our genome assembly is highly contiguous and is of similar quality to other bird genome assemblies.

genomics↗

Impacts of increasing isolation and environmental variation on Florida Scrub-Jay demography

Isolation caused by anthropogenic habitat fragmentation can destabilize populations. Populations relying on the inflow of immigrants can face reduced fitness due to inbreeding depression as fewer new individuals arrive. Empirical studies of the demographic consequences of isolation are critical to understand how populations persist through changing conditions. We used a 34-year demographic and environmental dataset from a population of cooperatively-breeding Florida Scrub-Jays (Aphelocoma coerulescens) to create mechanistic models linking environmental and demographic factors to population growth rates. We found that the population has not declined despite both declining immigration and increasing inbreeding, owing to a coinciding response in breeder survival. We find evidence of density-dependent immigration, breeder survival, and fecundity, indicating that interactions between vital rates and local density play a role in buffering the population against change. Our study elucidates the impacts of isolation on demography and how long-term stability is maintained via demographic responses.

ecology↗

Prospecting is physiologically costly in a resident cooperative breeder, the Florida scrub-jay

Prospecting is an understudied yet pivotal information-gathering process often preceding natal dispersal. While prospecting may enable individuals to optimise dispersal outcomes and obtain high quality territories, it is also likely to incur costs stemming from energy expenditure and predation risks. This trade-off may drive individual differences in prospecting effort. We tested for evidence of costs of prospecting behaviour in a wild population of Florida scrub-jays, Aphelocoma coerulescens, which prospect as nonbreeding helpers. Using random sampling across all helpers, we compared prospecting effort--approximated by frequency, distance, and activity level--with body mass changes and oxidative stress levels. We tested if prospecting incurred costs and if early-life body condition predicted subsequent prospecting effort. Prospecting frequency was positively linked to oxidative damage but not to any loss in body mass during the breeding season, suggesting that extra-territorial movement costs manifest unevenly. Early-stage body condition did not affect subsequent prospecting effort across a large set of helpers, but early-stage body condition and morphometric measures did correlate with subsequent oxidative status of those sampled. Our results suggest that prospecting movement carries some physiological costs, perhaps contributing to individual differences in prospecting. This research highlights how body condition plays a role in trade-offs between information gathering movement and physiological costs of movement itself, ultimately providing insight on the evolution of prospecting in social species. HIGHLIGHTSO_LIProspecting prior to breeding enables informed dispersal but incurs cost C_LIO_LIWe tested whether prospecting by nonbreeding Florida scrub-jays results in physiological costs or varies with initial condition C_LIO_LIWe measured oxidative status using assays testing antioxidant capacity and oxidative damage C_LIO_LIFrequent prospecting was linked to subsequent oxidative damage C_LIO_LIEarly-stage body condition and wing length affected subsequent oxidative status C_LI

ecology↗

Allele frequency dynamics under sex-biased demography and sex-specific inheritance in a pedigreed population

Sex-biased demography, including sex-biased survival or migration, can alter allele frequency changes across the genome. In particular, we can expect different patterns of genetic variation on autosomes and sex chromosomes due to sex-specific differences in life histories, as well as differences in effective population size, transmission modes, and the strength and mode of selection. Here, we demonstrate the role that sex differences in life history played in shaping short-term evolutionary dynamics across the genome. We used a 25-year pedigree and genomic dataset from a long-studied population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of sex-biased demography and inheritance in shaping genome-wide allele frequency trajectories. We used gene dropping simulations to estimate individual genetic contributions to future generations and to model drift and immigration on the known pedigree. We quantified differential expected genetic contributions of males and females over time, showing the impact of sex-biased dispersal in a monogamous system. Due to female-biased dispersal, more autosomal variation is introduced by female immigrants. However, due to male-biased transmission, more Z variation is introduced by male immigrants. Finally, we partitioned the proportion of variance in allele frequency change through time due to male and female contributions. Overall, most allele frequency change is due to variance in survival and births. Males and females make similar contributions to autosomal allele frequency change, but males make higher contributions to allele frequency change on the Z chromosome. Our work shows the importance of understanding sex-specific demographic processes in characterizing genome-wide allele frequency change in wild populations.

evolutionary biology↗

Allele frequency dynamics in a pedigreed natural population

A central goal of population genetics is to understand how genetic drift, natural selection, and gene flow shape allele frequencies through time. However, the actual processes underlying these changes - variation in individual survival, reproductive success, and movement - are often difficult to quantify. Fully understanding these processes requires the population pedigree, the set of relationships among all individuals in the population through time. Here, we use extensive pedigree and genomic information from a long-studied natural population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of different evolutionary processes in shaping patterns of genetic variation through time. We performed gene dropping simulations to estimate individual genetic contributions to the population and model drift on the known pedigree. We found that observed allele frequency changes are generally well predicted by accounting for the different genetic contributions of founders. Our results show that the genetic contribution of recent immigrants is substantial, with some large allele frequency shifts that otherwise may have been attributed to selection actually due to gene flow. We identified a few SNPs under directional short-term selection after appropriately accounting for gene flow. Using models that account for changes in population size, we partitioned the proportion of variance in allele frequency change through time. Observed allele frequency changes are primarily due to variation in survival and reproductive success, with gene flow making a smaller contribution. This study provides one of the most complete descriptions of short-term evolutionary change in allele frequencies in a natural population to date.

evolutionary biology↗

Deconstructing isolation-by-distance: the genomic consequences of limited dispersal

Geographically limited dispersal can shape genetic population structure and result in a correlation between genetic and geographic distance, commonly called isolation-bydistance. Despite the prevalence of isolation-by-distance in nature, to date few studies have empirically demonstrated the processes that generate this pattern, largely because few populations have direct measures of individual dispersal and pedigree information. Intensive, long-term demographic studies and exhaustive genomic surveys in the Florida Scrub-Jay (Aphelocoma coerulescens) provide an excellent opportunity to investigate the influence of dispersal on genetic structure. Here, we used a panel of genome-wide SNPs and extensive pedigree information to explore the role of limited dispersal in shaping patterns of isolation-by-distance in both sexes, and at an exceedingly fine spatial scale (within ~10 km). Isolation-by-distance patterns were stronger in male-male and male-female comparisons than in female-female comparisons, consistent with observed differences in dispersal propensity between the sexes. Using the pedigree, we demonstrated how various genealogical relationships contribute to fine-scale isolation-by-distance. Simulations using field-observed distributions of male and female natal dispersal distances showed good agreement with the distribution of geographic distances between breeding individuals of different pedigree relationship classes. Furthermore, we extended Malecots theory of isolation-by-distance by building coalescent simulations parameterized by the observed dispersal curve, population density, and immigration rate, and showed how incorporating these extensions allows us to accurately reconstruct observed sex-specific isolation-by-distance patterns in autosomal and Z-linked SNPs. Therefore, patterns of fine-scale isolation-by-distance in the Florida Scrub-Jay can be well understood as a result of limited dispersal over contemporary timescales.\n\nAuthor SummaryDispersal is a fundamental component of the life history of most organisms and therefore influences many biological processes. Dispersal is particularly important in creating genetic structure on the landscape. We often observe a pattern of decreased genetic relatedness between individuals as geographic distances increases, or isolation-by-distance. This pattern is particularly pronounced in organisms with extremely short dispersal distances. Despite the ubiquity of isolation-by-distance patterns in nature, there are few examples that explicitly demonstrate how limited dispersal influences spatial genetic structure. Here we investigate the processes that result in spatial genetic structure using the Florida Scrub-Jay, a bird with extremely limited dispersal behavior and extensive genome-wide data. We take advantage of the long-term monitoring of a contiguous population of Florida Scrub-Jays, which has resulted in a detailed pedigree and measurements of dispersal for hundreds of individuals. We show how limited dispersal results in close genealogical relatives living closer together geographically, which generates a strong pattern of isolation-by-distance at an extremely small spatial scale (<10 km) in just a few generations. Given the detailed dispersal, pedigree, and genomic data, we can achieve a fairly complete understanding of how dispersal shapes patterns of genetic diversity over short spatial scales.

evolutionary biology↗